Anti-spike IgG causes severe acute lung injury by skewing macrophage responses during acute SARS-CoV infection

Liu, Li; Wei, Qiang; Lin, Qingqing; Fang, Jun; Wang, Haibo; Kwok, Hauyee; Tang, Hangying; Nishiura, Kenji; Peng, Jie; Tan, Zhiwu; Wu, Tongjin; Cheung, Ka-Wai; Chan, Kwok-Hung; Alvarez, Xavier; Qin, Chuan; Lackner, Andrew; Perlman, Stanley; Yuen, Kwok-Yung; Chen, Zhiwei

doi:10.1172/jci.insight.123158

Cited by 830SARS-CoV-2 and COVID-19 ResearchCOVID-19 Clinical Research StudiesRespiratory Support and Mechanisms

Anti-spike IgG causes severe acute lung injury by skewing macrophage responses during acute SARS-CoV infection

Open access

Liu, Li, Wei, Qiang, Lin, Qingqing, Fang, Jun, Wang, Haibo, Kwok, Hauyee, Tang, Hangying, Nishiura, Kenji +11 more·2019·JCI Insight

DOI 10.1172/jci.insight.123158PMC PMC6478436

Open this paper in CoChat — free account Open PDF

Abstract

Newly emerging viruses, such as severe acute respiratory syndrome coronavirus (SARS-CoV), Middle Eastern respiratory syndrome CoVs (MERS-CoV), and H7N9, cause fatal acute lung injury (ALI) by driving hypercytokinemia and aggressive inflammation through mechanisms that remain elusive. In SARS-CoV/macaque models, we determined that anti-spike IgG (S-IgG), in productively infected lungs, causes severe ALI by skewing inflammation-resolving response. Alveolar macrophages underwent functional polarization in acutely infected macaques, demonstrating simultaneously both proinflammatory and wound-healing characteristics. The presence of S-IgG prior to viral clearance, however, abrogated wound-healing responses and promoted MCP1 and IL-8 production and proinflammatory monocyte/macrophage recruitment and accumulation. Critically, patients who eventually died of SARS (hereafter referred to as deceased patients) displayed similarly accumulated pulmonary proinflammatory, absence of wound-healing macrophages, and faster neutralizing antibody responses. Their sera enhanced SARS-CoV-induced MCP1 and IL-8 production by human monocyte-derived wound-healing macrophages, whereas blockade of FcγR reduced such effects. Our findings reveal a mechanism responsible for virus-mediated ALI, define a pathological consequence of viral specific antibody response, and provide a potential target for treatment of SARS-CoV or other virus-mediated lung injury.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1172/jci.insight.123158

Cites

53 of 53 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

S-specific IgG antibodies have been suggested to cause acute pulmonary injury in vaccine challenge animal models of SARS-CoV.
“S-specific IgG antibodies have been suggested to cause acute pulmonary injury in vaccine challenge animal models of SARS-CoV (Liu et al., 2019)”
From A thermostable mRNA vaccine against COVID-19 (2020) · cites this paper as Liu et al., 2019

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Exploring the full spectrum of macrophage activation
Mosser, D. M., & Edwards, J. P. (2008) · Nature Reviews Immunology · doi:10.1038/nri2448 · Cited by 9,144 · see citing works
Macrophage activation and polarization: nomenclature and experimental guidelines
Murray, P. J., Allen, J. E., Biswas, S. K., Fisher, E. A., Gilroy, D. W., Goerdt, S., Gordon, S., Hamilton, J. A., Ivashkiv, L. B., Lawrence, T., et al. (2014) · Immunity · doi:10.1016/j.immuni.2014.06.008 · Cited by 6,337 · see citing works
Protective and pathogenic functions of macrophage subsets
Murray, P. J., & Wynn, T. A. (2011) · Nature Reviews Immunology · doi:10.1038/nri3073 · Cited by 5,269 · see citing works
The Acute Respiratory Distress Syndrome
Matthay, M. A. (1996) · New England Journal of Medicine · doi:10.1056/nejm199605303342209 · Cited by 4,924 · see citing works
The Acute Respiratory Distress Syndrome
Ware, L. B., & Matthay, M. A. (2000) · New England Journal of Medicine · doi:10.1056/nejm200005043421806 · Cited by 4,666 · see citing works
Identification of a novel coronavirus in patients with severe acute respiratory syndrome
Drosten, C., Günther, S., Preiser, W., van der Werf, S., Brodt, H.-R., Becker, S., Rabenau, H., Panning, M., Kolesnikova, L., Fouchier, R. A. M., et al. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa030747 · Cited by 4,574 · see citing works
Macrophages in Tissue Repair, Regeneration, and Fibrosis
Wynn, T. A., & Vannella, K. M. (2016) · Immunity · doi:10.1016/j.immuni.2016.02.015 · Cited by 4,481 · see citing works
A Novel Coronavirus Associated with Severe Acute Respiratory Syndrome
Tg, K., Erdman, D. D., Cs, G., Zaki, Peret, T. C. T., Emery, S. L., Tong, S., Urbani, C., Comer, J. A., Lim, W., et al. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa030781 · Cited by 4,345 · see citing works
Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study
Peiris, J., Chu, C., Cheng, V., Chan, K., Hung, I., Poon, L., Law, K., Tang, B., Hon, T., Chan, C., et al. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13412-5 · Cited by 2,375 · see citing works
Self-citation
Dysregulated Type I Interferon and Inflammatory Monocyte-Macrophage Responses Cause Lethal Pneumonia in SARS-CoV-Infected Mice
Channappanavar, R., Fehr, A. R., Vijay, R., Mack, M., Zhao, J., Meyerholz, D. K., & Perlman, S. M. (2016) · Cell Host & Microbe · doi:10.1016/j.chom.2016.01.007 · Cited by 1,400 · see citing works
Self-citation
Identification of Oxidative Stress and Toll-like Receptor 4 Signaling as a Key Pathway of Acute Lung Injury
Imai, Y., Kuba, K., Neely, G. G., Yaghubian-Malhami, R., Perkmann, T., van Loo, G., Ermolaeva, M., Veldhuizen, R., Leung, Y. H. C., Wang, H., et al. (2008) · Cell · doi:10.1016/j.cell.2008.02.043 · Cited by 1,356 · see citing works
Self-citation
Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo
Atreya, R., Mudter, J., Finotto, S., Müllberg, J., Jostock, T., Wirtz, S., Schütz, M., Bartsch, B., Holtmann, M., Becker, C., et al. (2000) · Nature Medicine · doi:10.1038/75068 · Cited by 1,293 · see citing works
The Effectiveness of Convalescent Plasma and Hyperimmune Immunoglobulin for the Treatment of Severe Acute Respiratory Infections of Viral Etiology: A Systematic Review and Exploratory Meta-analysis
Mair-Jenkins, J., Saavedra-Campos, M., Baillie, J. K., Cleary, P. R., Khaw, F.-M., Lim, W. S., Makki, S., Rooney, K., Convalescent Plasma Study Group, Nguyen‐Van‐Tam, J. S., et al. (2014) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiu396 · Cited by 985 · see citing works
Use of convalescent plasma therapy in SARS patients in Hong Kong
Cheng, Y., Wong, R. S. M., Soo, Y. O. Y., Wong, W. S., Lee, C. K., Ng, M. H. L., Chan, P. K. S., Wong, K. C., Leung, C. B., & Cheng, G. Y.-M. (2004) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-004-1271-9 · Cited by 953 · see citing works
A DNA vaccine induces SARS coronavirus neutralization and protective immunity in mice
Yang, Z.-Y., Kong, W., Huang, Y., Roberts, A., Murphy, B., Subbarao, K., & Nabel, G. (2004) · Nature · doi:10.1038/nature02463 · Cited by 688 · see citing works
Immunization with SARS Coronavirus Vaccines Leads to Pulmonary Immunopathology on Challenge with the SARS Virus
Tseng, C.-T. K., Sbrana, E., Iwata‐Yoshikawa, N., Newman, P. C., Garron, T. M., Atmar, R. L., Peters, C. J., & Couch, R. B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035421 · Cited by 555 · see citing works
Immunopathogenesis of coronavirus infections: implications for SARS
Dandekar, A. A., & Perlman, S. M. (2005) · Nature reviews. Immunology · doi:10.1038/nri1732 · Cited by 499 · see citing works
Self-citation
Airway Memory CD4+ T Cells Mediate Protective Immunity against Emerging Respiratory Coronaviruses
Zhao, J., Zhao, J., Mangalam, A. K., Channappanavar, R., Fett, C., Meyerholz, D. K., Agnihothram, S., Baric, R. S., David, C. S., & Perlman, S. (2016) · Immunity · doi:10.1016/j.immuni.2016.05.006 · Cited by 496 · see citing works
Self-citation
A Double-Inactivated Severe Acute Respiratory Syndrome Coronavirus Vaccine Provides Incomplete Protection in Mice and Induces Increased Eosinophilic Proinflammatory Pulmonary Response upon Challenge
Bolles, M., Deming, D., Long, K., Agnihothram, S., Whitmore, A., Ferris, M., Funkhouser, W., Gralinski, L., Totura, A., Heise, M., et al. (2011) · Journal of Virology · doi:10.1128/jvi.06048-11 · Cited by 477 · see citing works
Using siRNA in prophylactic and therapeutic regimens against SARS coronavirus in Rhesus macaque
Li, B.-J., Tang, Q., Cheng, D., Qin, C., Xie, F. Y., Wei, Q., Xu, J., Liu, Y., Zheng, B.-J., Woodle, M. C., et al. (2005) · Nature Medicine · doi:10.1038/nm1280 · Cited by 433 · see citing works
Self-citation
Virus-specific memory CD8 T cells provide substantial protection from lethal severe acute respiratory syndrome coronavirus infection
Channappanavar, R., Fett, C., Zhao, J., Meyerholz, D. K., & Perlman, S. (2014) · Journal of Virology · doi:10.1128/jvi.01505-14 · Cited by 411 · see citing works
Prior Infection and Passive Transfer of Neutralizing Antibody Prevent Replication of Severe Acute Respiratory Syndrome Coronavirus in the Respiratory Tract of Mice
Subbarao, K., McAuliffe, J. M., Vogel, L., Fahle, G. A., Fischer, S. H., Tatti, K. M., Packard, M. M., Shieh, W., Zaki, S. R., & Murphy, B. R. (2004) · Journal of Virology · doi:10.1128/jvi.78.7.3572-3577.2004 · Cited by 397 · see citing works
Retrospective comparison of convalescent plasma with continuing high-dose methylprednisolone treatment in SARS patients
Soo, Y. O. Y., Cheng, Y., Wong, R. S. M., Hui, D. S. C., Lee, C. K., Tsang, K., Ng, M., Chan, P. K. S., Cheng, G. Y.-M., & Sung, J. J. �. (2004) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2004.00956.x · Cited by 381 · see citing works
Regulating the adaptive immune response to respiratory virus infection
Braciale, T. J., Sun, J., & Kim, T. S. (2012) · Nature reviews. Immunology · doi:10.1038/nri3166 · Cited by 362 · see citing works
T Cell Responses Are Required for Protection from Clinical Disease and for Virus Clearance in Severe Acute Respiratory Syndrome Coronavirus-Infected Mice
Zhao, J., Zhao, J., & Perlman, S. (2010) · Journal of Virology · doi:10.1128/jvi.01049-10 · Cited by 340 · see citing works
Self-citation
Pulmonary pathology of severe acute respiratory syndrome in Toronto
Hwang, D. M., Chamberlain, D. W., Poutanen, S. M., Low, D. E., Asa, S. L., & Butany, J. (2005) · Modern Pathology · doi:10.1038/modpathol.3800247 · Cited by 332 · see citing works
Acute Lung Injury: How Macrophages Orchestrate Resolution of Inflammation and Tissue Repair
Herold, S., Mayer, K., & Lohmeyer, J. (2011) · Frontiers in Immunology · doi:10.3389/fimmu.2011.00065 · Cited by 331 · see citing works
Immunodominant SARS Coronavirus Epitopes in Humans Elicited both Enhancing and Neutralizing Effects on Infection in Non-human Primates
Wang, Q., Zhang, L., Kuwahara, K., Li, L., Liu, Z., Li, T., Zhu, H., Liu, J., Xu, Y., Xie, J., et al. (2016) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.6b00006 · Cited by 297 · see citing works
Self-citation
Immune Responses and Disease Enhancement during Respiratory Syncytial Virus Infection
Openshaw, P., & Tregoning, J. S. (2005) · Clinical Microbiology Reviews · doi:10.1128/cmr.18.3.541-555.2005 · Cited by 293 · see citing works
Severe pandemic 2009 H1N1 influenza disease due to pathogenic immune complexes
Monsalvo, A. C., Batalle, J. P., López, M. G., Krause, J. C., Klemenc, J. M., Hernandez, J. Z., Maskin, B. C., Bugna, J., Rubinstein, C. J., Aguilar, L., et al. (2010) · Nature Medicine · doi:10.1038/nm.2262 · Cited by 263 · see citing works
Severe Acute Respiratory Syndrome-Associated Coronavirus Vaccines Formulated with Delta Inulin Adjuvants Provide Enhanced Protection while Ameliorating Lung Eosinophilic Immunopathology
Honda‐Okubo, Y., Barnard, D. L., Ong, C. H., Peng, B., Tseng, C.-T. K., & Petrovsky, N. (2014) · Journal of Virology · doi:10.1128/jvi.02980-14 · Cited by 204 · see citing works
In Vivo Characterization of Alveolar and Interstitial Lung Macrophages in Rhesus Macaques: Implications for Understanding Lung Disease in Humans
Cai, Y., Sugimoto, C., Araínga, M., Alvarez, X. A., Didier, E. S., & Kuroda, M. J. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302269 · Cited by 201 · see citing works
Self-citation
Antibody responses against SARS coronavirus are correlated with disease outcome of infected individuals
Zhang, L., Zhang, F., Yu, W., Tian, H., Yu, J., Yi, C. E., Ba, L., Li, W., Farzan, M., Chen, Z., et al. (2005) · Journal of Medical Virology · doi:10.1002/jmv.20499 · Cited by 184 · see citing works
Self-citation
Receptor-binding domain of SARS-CoV spike protein induces long-term protective immunity in an animal model
Du, L., Zhao, G., He, Y., Guo, Y., Zheng, B., Jiang, S., & Zhou, Y. (2006) · Vaccine · doi:10.1016/j.vaccine.2006.10.031 · Cited by 182 · see citing works
Recombinant Modified Vaccinia Virus Ankara Expressing the Spike Glycoprotein of Severe Acute Respiratory Syndrome Coronavirus Induces Protective Neutralizing Antibodies Primarily Targeting the Receptor Binding Region
Chen, Z., Zhang, L., Qin, C., Ba, L., Yi, C. E., Zhang, F., Wei, Q., Tian, H., Yu, W., Yu, J., et al. (2005) · Journal of Virology · doi:10.1128/jvi.79.5.2678-2688.2005 · Cited by 181 · see citing works
Self-citation
Intranasal Vaccination of Recombinant Adeno-Associated Virus Encoding Receptor-Binding Domain of Severe Acute Respiratory Syndrome Coronavirus (SARS-CoV) Spike Protein Induces Strong Mucosal Immune Responses and Provides Long-Term Protection against SARS-CoV Infection
Du, L., Zhao, G., Lin, Y., Sui, H., Chan, C. C. S., Ma, S., He, Y., Jiang, S., Wu, C. Y., Yuen, K., et al. (2008) · The Journal of Immunology · doi:10.4049/jimmunol.180.2.948 · Cited by 136 · see citing works
Self-citation
Recently Infiltrating MAC387+ Monocytes/Macrophages
Soulas, C., Conerly, C. N., Kim, W., Burdo, T. H., Alvarez, X. A., Lackner, A. A., & Williams, K. C. (2011) · American Journal Of Pathology · doi:10.1016/j.ajpath.2011.01.023 · Cited by 130 · see citing works
Self-citation
Effects of Toll-Like Receptor Stimulation on Eosinophilic Infiltration in Lungs of BALB/c Mice Immunized with UV-Inactivated Severe Acute Respiratory Syndrome-Related Coronavirus Vaccine
Iwata‐Yoshikawa, N., Uda, A., Suzuki, T., Tsunetsugu‐Yokota, Y., Sato, Y., Morikawa, S., Tashiro, M., Sata, T., Hasegawa, H., & Nagata, N. (2014) · Journal of Virology · doi:10.1128/jvi.00983-14 · Cited by 130 · see citing works
Severe Acute Respiratory Syndrome in Children
Stockman, L. J., Massoudi, M. S., Helfand, R. F., Erdman, D. D., Siwek, A. M., Anderson, L. J., & Parashar, U. D. (2006) · The Pediatric Infectious Disease Journal · doi:10.1097/01.inf.0000247136.28950.41 · Cited by 120 · see citing works
Complete Protection against Severe Acute Respiratory Syndrome Coronavirus-Mediated Lethal Respiratory Disease in Aged Mice by Immunization with a Mouse-Adapted Virus Lacking E Protein
Fett, C., DeDiego, M. L., Regla-Nava, J. Á., Enjuanes, L., & Perlman, S. M. (2013) · Journal of Virology · doi:10.1128/jvi.00087-13 · Cited by 118 · see citing works
Self-citation
SARS: clinical virology and pathogenesis
Nicholls, J. M., Dong, X., Gu, J., & Peiris, M. J. S. (2003) · Respirology · doi:10.1046/j.1440-1843.2003.00517.x · Cited by 98 · see citing works
An animal model of SARS produced by infection of Macaca mulatta with SARS coronavirus
Qin, C., Wang, J., Wei, Q., She, M., Marasco, W. A., Jiang, H., Tu, X., Zhu, H., Ren, L., Gao, H., et al. (2005) · The Journal of Pathology · doi:10.1002/path.1769 · Cited by 96 · see citing works
Self-citation
Macrophages inhibit human osteosarcoma cell growth after activation with the bacterial cell wall derivative liposomal muramyl tripeptide in combination with interferon-γ
Pahl, J. H., Kwappenberg, K., Varypataki, E., Santos, S., Kuijjer, M., Mohamed, S., Wijnen, J., van Tol, M. V., Cleton-Jansen, A., Egeler, R., et al. (2014) · Journal of experimental & clinical cancer research : CR · doi:10.1186/1756-9966-33-27 · Cited by 94 · see citing works
Priming with rAAV encoding RBD of SARS-CoV S protein and boosting with RBD-specific peptides for T cell epitopes elevated humoral and cellular immune responses against SARS-CoV infection
Du, L., Zhao, G., Lin, Y., Chan, C. C. S., He, Y., Jiang, S., Wu, C. Y., Jin, D., Yuen, K., Zhou, Y., et al. (2008) · Vaccine · doi:10.1016/j.vaccine.2008.01.025 · Cited by 86 · see citing works
Self-citation
High Titer and Avidity of Nonneutralizing Antibodies against Influenza Vaccine Antigen Are Associated with Severe Influenza
To, K. K., Zhang, J., Hung, I. F., Xu, T., Ip, W. C., Wong, R. T. Y., Ng, J. C. K., Chan, J. F., Chan, K., & Yuen, K. (2012) · Clinical and Vaccine Immunology · doi:10.1128/cvi.00081-12 · Cited by 83 · see citing works
Self-citation
Immunogenicity, safety, and protective efficacy of an inactivated SARS-associated coronavirus vaccine in rhesus monkeys
Zhou, J., Wang, W., Zhong, Q., Hou, W., Yang, Z., Xiao, S., Runqing, Z., Tang, Z., Wang, Y., Xian, Q., et al. (2005) · Vaccine · doi:10.1016/j.vaccine.2004.11.075 · Cited by 78 · see citing works
Self-citation
Immunogenicity and protective efficacy in monkeys of purified inactivated Vero-cell SARS vaccine
Qin, E.-D., Shi, H., Tang, L., Wang, C., Chang, G., Ding, Z., Zhao, K., Wang, J., Chen, Z., Yu, M., et al. (2005) · Vaccine · doi:10.1016/j.vaccine.2005.06.038 · Cited by 75 · see citing works
Self-citation
Primary Severe Acute Respiratory Syndrome Coronavirus Infection Limits Replication but Not Lung Inflammation upon Homologous Rechallenge
Clay, C. C., Donart, N., Fomukong, N. G., Knight, J. B., Lei, W., Price, L., Hahn, F. F., Westrienen, J. V., & Harrod, K. S. (2012) · Journal of Virology · doi:10.1128/jvi.06791-11 · Cited by 64 · see citing works
Single Amino Acid Substitutions in the Severe Acute Respiratory Syndrome Coronavirus Spike Glycoprotein Determine Viral Entry and Immunogenicity of a Major Neutralizing Domain
Yi, C. E., Ba, L., Zhang, L., Ho, D. D., & Chen, Z. (2005) · Journal of Virology · doi:10.1128/jvi.79.18.11638-11646.2005 · Cited by 63 · see citing works
Self-citation
Spatiotemporal interplay of severe acute respiratory syndrome coronavirus and respiratory mucosal cells drives viral dissemination in rhesus macaques
Liu, L., Wei, Q., Nishiura, K., et al. (2015) · Mucosal Immunology · doi:10.1038/mi.2015.127 · Cited by 45 · see citing works
Self-citation
The Relative Efficacy of Boceprevir and Telaprevir in the Treatment of Hepatitis C Virus Genotype 1
Kieran, J., Schmitz, S., O’Leary, A. C., et al. (2012) · Clinical Infectious Diseases · doi:10.1093/cid/cis880 · Cited by 27 · see citing works
Confronting SARS: a view from Hong Kong
Peiris, M. J. S., & Guan, Y. (2004) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2004.1482 · Cited by 23 · see citing works
Monoclonal antibodies specific to human Δ42PD1: A novel immunoregulator potentially involved in HIV-1 and tumor pathogenesis
Cheng, L. Z., Tang, X., Liu, L., Peng, J., Nishiura, K., Cheung, A. K. L., Guo, J., Wu, X., Tang, H. Y., An, M., et al. (2015) · mAbs · doi:10.1080/19420862.2015.1016695 · Cited by 11 · see citing works
Self-citation

Flagged first, then by citations

Sorted by citations

The trinity of COVID-19: immunity, inflammation and intervention
Tay, M. Z., Poh, C. M., Rénia, L., MacAry, P. A., & Ng, L. F. P. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-020-0311-8 · Cited by 4,360 · see citing works
Targets of T Cell Responses to SARS-CoV-2 Coronavirus in Humans with COVID-19 Disease and Unexposed Individuals
Grifoni, A., Weiskopf, D., Ramirez, S. I., Mateus, J., Dan, J. M., Moderbacher, C. R., Rawlings, S. A., Sutherland, A., Premkumar, L., Jadi, R. S., et al. (2020) · Cell · doi:10.1016/j.cell.2020.05.015 · Cited by 3,595 · see citing works
Safety and immunogenicity of the ChAdOx1 nCoV-19 vaccine against SARS-CoV-2: a preliminary report of a phase 1/2, single-blind, randomised controlled trial
Folegatti, P. M., Ewer, K. J., Aley, P. K., Angus, B., Becker, S., Belij-Rammerstorfer, S., Bellamy, D., Bibi, S., Bittaye, M., Clutterbuck, E. A., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)31604-4 · Cited by 2,419 · see citing works
Antibody Responses to SARS-CoV-2 in Patients With Novel Coronavirus Disease 2019
Zhao, J., Yuan, Q., Wang, H., Liu, W., Liao, X., Su, Y., Wang, X., Yuan, J., Li, T., Li, J., et al. (2020) · Clinical Infectious Diseases · doi:10.1093/cid/ciaa344 · Cited by 2,607 · see citing works
Self-citation
Pathological inflammation in patients with COVID-19: a key role for monocytes and macrophages
Merad, M., & Martin, J. C. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-020-0331-4 · Cited by 2,472 · see citing works
Immunology of COVID-19: Current State of the Science
Vabret, N., Britton, G. J., Gruber, C., Hegde, S., Kim, J., Kuksin, M., Levantovsky, R., Malle, L., Moreira, A., Park, M. D., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.05.002 · Cited by 1,623 · see citing works
Distinct conformational states of SARS-CoV-2 spike protein
Cai, Y., Zhang, J., Xiao, T., Peng, H., Sterling, S. M., Walsh, R. M., Rawson, S., Rits-Volloch, S., & Chen, B. (2020) · Science · doi:10.1126/science.abd4251 · Cited by 1,221 · see citing works
Why does COVID-19 disproportionately affect older people?
Mueller, A. L., McNamara, M. S., & Sinclair, D. A. (2020) · Aging · doi:10.18632/aging.103344 · Cited by 1,128 · see citing works
DNA vaccine protection against SARS-CoV-2 in rhesus macaques
Yu, J., Tostanoski, L. H., Peter, L., Mercado, N. B., McMahan, K., Mahrokhian, S. H., Nkolola, J. P., Liu, J., Li, Z., Chandrashekar, A., et al. (2020) · Science · doi:10.1126/science.abc6284 · Cited by 997 · see citing works
ChAdOx1 nCoV-19 vaccine prevents SARS-CoV-2 pneumonia in rhesus macaques
van Doremalen, N., Lambe, T., Spencer, A., Belij-Rammerstorfer, S., Purushotham, J. N., Port, J. R., Avanzato, V. A., Bushmaker, T., Flaxman, A., Ulaszewska, M., et al. (2020) · Nature · doi:10.1038/s41586-020-2608-y · Cited by 914 · see citing works
Immunological considerations for COVID-19 vaccine strategies
Jeyanathan, M., Afkhami, S., Smaill, F., Miller, M. S., Lichty, B. D., & Xing, Z. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-020-00434-6 · Cited by 1,015 · see citing works
Coronavirus Disease 2019 (COVID-19) Re-infection by a Phylogenetically Distinct Severe Acute Respiratory Syndrome Coronavirus 2 Strain Confirmed by Whole Genome Sequencing
To, K. K.-W., Hung, I. F.-N., Ip, J. D., Chu, A. W.-H., Chan, W.-M., Tam, A. R., Fong, C. H.-Y., Yuan, S., Tsoi, H.-W., Ng, A. C.-K., et al. (2021) · Clinical Infectious Diseases · doi:10.1093/cid/ciaa1275 · Cited by 746 · see citing works
Self-citation
Antibody-dependent enhancement and SARS-CoV-2 vaccines and therapies
Lee, W. S., Wheatley, A. K., Kent, S. J., & DeKosky, B. J. (2020) · Nature Microbiology · doi:10.1038/s41564-020-00789-5 · Cited by 676 · see citing works
A thermostable mRNA vaccine against COVID-19
Zhang, N.-N., Li, X.-F., Deng, Y.-Q., Zhao, H., Huang, Y.-J., Yang, G., Huang, W.-J., Gao, P., Zhou, C., Zhang, R.-R., et al. (2020) · Cell · doi:10.1016/j.cell.2020.07.024 · Cited by 671 · see citing works
“d Development of LNP-encapsulated mRNA vaccine (ARCoV) targeting the RBD of SARS-CoV-2 d ARCoV induces neutralizing antibodies and T cell immunity in mice and NHPs d ARCoV vaccination confers full protection against SARS- CoV-2 challenge in mice d ARCoV is a thermostable vaccine candidate for phase I studies Zhang et…”
InfluentialSelf-citation
SARS-CoV-2-derived peptides define heterologous and COVID-19-induced T cell recognition
Nelde, A., Bilich, T., Heitmann, J. S., Maringer, Y., Salih, H. R., Roerden, M., Lübke, M., Bauer, J., Rieth, J., Wacker, M., et al. (2021) · Nature Immunology · doi:10.1038/s41590-020-00808-x · Cited by 582 · see citing works
Acute SARS-CoV-2 Infection Impairs Dendritic Cell and T Cell Responses
Zhou, R., To, K. K.-W., Wong, Y.-C., Liu, L., Zhou, B., Li, X., Huang, H., Mo, Y., Luk, T.-Y., Lau, T. T.-K., et al. (2020) · Immunity · doi:10.1016/j.immuni.2020.07.026 · Cited by 531 · see citing works
Self-citation
Host-Viral Infection Maps Reveal Signatures of Severe COVID-19 Patients
Bost, P., Giladi, A., Liu, Y., Bendjelal, Y., Xu, G., David, E., Blecher-Gonen, R., Cohen, M., Medaglia, C., Li, H., et al. (2020) · Cell · doi:10.1016/j.cell.2020.05.006 · Cited by 471 · see citing works
SARS-CoV-2 spike glycoprotein vaccine candidate NVX-CoV2373 immunogenicity in baboons and protection in mice
Tian, J.-H., Patel, N., Haupt, R., Zhou, H., Weston, S., Hammond, H., Logue, J., Portnoff, A. D., Norton, J., Guebre-Xabier, M., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20653-8 · Cited by 508 · see citing works
Peripheral immunophenotypes in children with multisystem inflammatory syndrome associated with SARS-CoV-2 infection
Carter, M. J., Fish, M., Jennings, A., Doores, K. J., Wellman, P., Seow, J., Acors, S., Graham, C., Timms, E., Kenny, J., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-1054-6 · Cited by 419 · see citing works
Clinical, molecular, and epidemiological characterization of the SARS-CoV-2 virus and the Coronavirus Disease 2019 (COVID-19), a comprehensive literature review
Ortiz-Prado, E., Simbaña-Rivera, K., Gómez- Barreno, L., Rubio-Neira, M., Guaman, L. P., Kyriakidis, N. C., Muslin, C., Jaramillo, A. M. G., Barba-Ostria, C., Cevallos-Robalino, D., et al. (2020) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2020.115094 · Cited by 458 · see citing works
Dysregulation of type I interferon responses in COVID-19
Acharya, D., Liu, G., & Gack, M. U. (2020) · Nature Reviews Immunology · doi:10.1038/s41577-020-0346-x · Cited by 454 · see citing works
Afucosylated IgG characterizes enveloped viral responses and correlates with COVID-19 severity
Larsen, M. D., de Graaf, E. L., Sonneveld, M. E., Plomp, H. R., Nouta, J., Hoepel, W., Chen, H.-J., Linty, F., Visser, R., Brinkhaus, M., et al. (2021) · Science · doi:10.1126/science.abc8378 · Cited by 408 · see citing works
COVID-19 vaccines: The status and perspectives in delivery points of view
Chung, J. Y., Thone, M. N., & Kwon, Y. J. (2021) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2020.12.011 · Cited by 375 · see citing works
Lessons for COVID-19 immunity from other coronavirus infections
Sariol, A., & Perlman, S. (2020) · Immunity · doi:10.1016/j.immuni.2020.07.005 · Cited by 317 · see citing works
Self-citation
The role of host genetics in the immune response to SARS-CoV-2 and COVID-19 susceptibility and severity
Ovsyannikova, I. G., Haralambieva, I. H., Crooke, S. N., Poland, G. A., & Kennedy, R. B. (2020) · Immunological Reviews · doi:10.1111/imr.12897 · Cited by 258 · see citing works
Prospects for a safe COVID-19 vaccine
Haynes, B. F., Corey, L., Fernandes, P., Gilbert, P. B., Hotez, P. J., Rao, S., Santos, M. R., Schuitemaker, H., Watson, M., & Arvin, A. (2020) · Science Translational Medicine · doi:10.1126/scitranslmed.abe0948 · Cited by 261 · see citing works
Consensus summary report for CEPI/BC March 12–13, 2020 meeting: Assessment of risk of disease enhancement with COVID-19 vaccines
Lambert, P.-H., Ambrosino, D. M., Andersen, S. R., Baric, R. S., Black, S. B., Chen, R. T., Dekker, C. L., Didierlaurent, A. M., Graham, B. S., Martin, S. D., et al. (2020) · Vaccine · doi:10.1016/j.vaccine.2020.05.064 · Cited by 119 · see citing works
Self-citation
Immunization with the receptor-binding domain of SARS-CoV-2 elicits antibodies cross-neutralizing SARS-CoV-2 and SARS-CoV without antibody-dependent enhancement
Zang, J., Gu, C., Zhou, B., Zhang, C., Yang, Y., Xu, S., Bai, L., Zhang, R., Deng, Q., Yuan, Z., et al. (2020) · Cell Discovery · doi:10.1038/s41421-020-00199-1 · Cited by 67 · see citing works
Self-citation
Recovery from COVID-19 in a B-cell-depleted multiple sclerosis patient
Wurm, H., Attfield, K., Iversen, A. K., Gold, R., Fugger, L., & Haghikia, A. (2020) · Multiple Sclerosis Journal · doi:10.1177/1352458520943791 · Cited by 36 · see citing works
A review of COVID-19 convalescent plasma use in COVID-19 with focus on proof of efficacy
Devarasetti, P. K., Rajasekhar, L., Baisya, R., Sreejitha, K. S., & Vardhan, Y. K. (2021) · Immunologic Research · doi:10.1007/s12026-020-09169-x · Cited by 17 · see citing works

Artificially induced in situ macrophage polarization: An emerging cellular therapy for immuno-inflammatory diseases
Chatterjee, O., & Sur, D. (2023) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2023.176006 · Cited by 19 · see citing works
FUCOIDIN INHIBITS OXIDIZED LOW DENSITY LIPOPROTEIN FROM INDUCING HUMAN PERIPHERAL BLOOD MONOCYTE EXPRESSION OF PROINFLAMMATORY CYTOKINES mRNA
雷新军, 马爱群, 任冰稳, et al. (2003) · 西安交通大学学报：英文版
Monocyte/Macrophage——atherapeutic target of atherosclerosis
Chen, F. (2011)
Macrophage polarization in atherosclerosis
Yang, S., Yuan, H., Hao, Y., Ren, Z., Qu, S.-L., Liu, L., Wei, D., Tang, Z., Zhang, J., & Jiang, Z. (2019) · Clinica Chimica Acta · doi:10.1016/j.cca.2019.10.034 · Cited by 219 · see citing works
Self-citation
LRG1 promotes atherosclerosis by inducing macrophage M1-like polarization
Wang, J., Wang, J., Zhong, J., Liu, H., Li, W., Chen, M., Xu, L. N., Zhang, W., Zhang, Z., Wei, Z., et al. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2405845121 · Cited by 35 · see citing works

Authors: Liu, L., Wei, Q., Lin, Q., Fang, J., Wang, H., Kwok, H., Tang, H., Nishiura, K., Peng, J., Tan, Z., Wu, T., Cheung, K.-W., Chan, K.-H., Alvarez, X., Qin, C., Lackner, A., Perlman, S., Yuen, K.-Y., & Chen, Z.
Affiliations: Shenzhen Third People’s Hospital (CN)
Chinese Academy of Medical Sciences & Peking Union Medical College (CN)
University of Hong Kong (HK)
Tulane University (US)
University of Iowa (US)
Corresponding author: Liu, Li
Chen, Zhiwei
ORCID: Liu, Li
Wei, Qiang
Lin, Qingqing
Fang, Jun
Wang, Haibo
Nishiura, Kenji
Peng, Jie
Tan, Zhiwu
Wu, Tongjin
Chan, Kwok-Hung
Alvarez, Xavier
Qin, Chuan
Lackner, Andrew
Perlman, Stanley
Yuen, Kwok-Yung
Chen, Zhiwei
Venue: JCI Insight
Publisher: American Society for Clinical Investigation
Published: 2019-02-21
Volume: 4
Issue: 4
ISSN: 2379-3708 (ISSN-L)
DOI: 10.1172/jci.insight.123158
PMC: PMC6478436
OpenAlex: W2915839491
Cited by: 830
References: 53
Citations by year: 2026: 7 · 2025: 14 · 2024: 27 · 2023: 46 · 2022: 101 · 2021: 246 · 2020: 387 · 2019: 1
FWCI: 140.99
Type: journal article
Language: en
Open access: gold
doi.org
Locations: JCI Insight (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: U.S. NIH , TNPRC, University Development Fund/Li Ka Shing Faculty of Medicine Matching Fund of the University of Hong Kong (RO1HL080211,RR00164,RO1060699)
Topics: Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Respiratory Support and Mechanisms
Keywords: SARS-CoV, acute lung injury, anti-spike IgG, alveolar macrophages, macrophage polarization, MCP-1, interleukin-8, Fc gamma receptor, neutralizing antibodies, cytokine storm, viral infection, macaque model, monocyte recruitment
MeSH terms: Adult, Aged, Aged, 80 and over, Animals, Antibodies, Viral, Cell Line, Disease Models, Animal, Female, Humans, Immunoglobulin G, Immunization, Passive, Lung, Macaca mulatta, Male, Middle Aged, Vaccinia virus, Viral Vaccines, Macrophages, Alveolar, Severe Acute Respiratory Syndrome, Severe acute respiratory syndrome-related coronavirus, Acute Lung Injury, Young Adult, Antibodies, Neutralizing, Spike Glycoprotein, Coronavirus

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Anti-spike IgG causes severe acute lung injury by skewing macrophage responses during acute SARS-CoV infection

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks